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. 2020 Mar 11:9:e51760.
doi: 10.7554/eLife.51760.

Energetic and physical limitations on the breaching performance of large whales

Paolo S Segre  1 , Jean Potvin  2 , David E Cade  1 , John Calambokidis  3 , Jacopo Di Clemente  4 , Frank E Fish  5 , Ari S Friedlaender  6 , William T Gough  1 , Shirel R Kahane-Rapport  1 , Cláudia Oliveira  7 , Susan E Parks  8 , Gwenith S Penry  9 , Malene Simon  10 , Alison K Stimpert  11 , David N Wiley  12 , K C Bierlich  13 , Peter T Madsen  14   15 , Jeremy A Goldbogen  1
Affiliations

Energetic and physical limitations on the breaching performance of large whales

Paolo S Segre et al. Elife. .

Abstract

The considerable power needed for large whales to leap out of the water may represent the single most expensive burst maneuver found in nature. However, the mechanics and energetic costs associated with the breaching behaviors of large whales remain poorly understood. In this study we deployed whale-borne tags to measure the kinematics of breaching to test the hypothesis that these spectacular aerial displays are metabolically expensive. We found that breaching whales use variable underwater trajectories, and that high-emergence breaches are faster and require more energy than predatory lunges. The most expensive breaches approach the upper limits of vertebrate muscle performance, and the energetic cost of breaching is high enough that repeated breaching events may serve as honest signaling of body condition. Furthermore, the confluence of muscle contractile properties, hydrodynamics, and the high speeds required likely impose an upper limit to the body size and effectiveness of breaching whales.

Keywords: breaching; cetaceans; locomotion; maneuverability; performance; physics of living systems.

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Conflict of interest statement

PS, JP, DC, JC, JD, FF, AF, WG, SK, CO, SP, GP, MS, AS, DW, KB, PM, JG No competing interests declared

Figures

Figure 1.
Figure 1.. Breaching whales.
(A) A tagged humpback whale (NMFS permit #16111). (B) A tagged humpback calf (NMFS permit #14682). (C) A tagged minke whale (NMFS permit #14809). (D) An untagged Bryde's whale breaching (credit K. Underhill, Simon's Town Boat Company). (E) A tagged gray whale falling back into the water (NMFS permit #16111). (F) An untagged sperm whale (permit #49/2010/DRA). (G) A tagged right whale (MMPA permit #775–1875). (H) An untagged blue whale partially emerging from the water while participating in a 'racing behavior' (NMFS permit #16111).
Figure 2.
Figure 2.. Representative breaching kinematics of a humpback whale.
Three metrics of pitch are shown: the pitch changes of the body (red), pitch oscillations due to the fluke stroke (orange), and the sum of the two (blue). Two measurements of speed are shown: speed calculated from orientation corrected depth rate (purple), and speed calculated from the accelerometer vibrations (blue). Depth is also shown (black). Images from the onboard camera are shown at specific landmarks during the breach. The video of this breach is included in the supplementary materials (Video 1).
Figure 3.
Figure 3.. The diversity of underwater breaching behavior is illustrated by the depth profiles of 152 breaching accelerations performed by 37 humpback whales.
Four representative trajectories illustrating U, V, I, and J-shaped breaching profiles are highlighted, showing both the beginning of the upwards acceleration (solid line) and the 16 s prior to the breach, provided for context (dotted line).
Figure 4.
Figure 4.. Representative breaching kinematics of a minke whale (A), a Bryde’s whale (B), a gray whale (C), a sperm whale (D), and a right whale (E).
Three metrics of pitch are shown: the pitch changes of the body (red), pitch oscillations due to the fluke stroke (orange), and the sum of the two (blue). Two measurements of speed are shown: speed calculated from orientation corrected depth rate (purple), and speed calculated from the accelerometer vibrations (blue). Depth is also shown (black). The graphs show the 12 s before the whale emerges from the water, with gray shaded areas representing time before the breaching maneuver begins.
Figure 5.
Figure 5.. Breaching speed is correlated with starting depth (A) and average stroke frequency (B), but not with breaching pitch (C), or breaching roll angle (D).
Figure 6.
Figure 6.. The cost of breaching increases with body size, in humpback whales.
(A) The mass-specific energy expenditure required to perform high-emergence breaches (blue) and high-performance lunges (red) is shown for five humpback whales of different sizes. Because the whales breached with different percentages of their bodies emerging from the water (dark blue numbers), the expected relationship between mass and the energetic cost of breaching with 80% body emergence, is shown for comparison (light blue line). The modeled breaches were calculated using average parameters from the trajectories of the five individuals shown (65° pitch; body width = 18% of length; 1.75 m/s starting velocity; 0.65 m/s2 acceleration; no plateau phase). Both the model and the data show that the mass-specific cost of breaching increases with body size. (B) This pattern is largely driven by the higher speeds that larger whales need to emerge from the water. (C) To attain the higher speeds required to emerge from the water, larger whales need to generate higher mass-specific mechanical power outputs or extend the duration of their trajectories (green numbers).
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